Anterior periventricular linear lesions in optic-spinal multiple sclerosis: a combined neuroimaging and neuropathological study

Abstract

There are two distinct subtypes of multiple sclerosis (MS) in Asians, optic-spinal (OSMS) and conventional (CMS). In OSMS, severe spinal cord lesions are characteristic while brain lesions are scant. We sought to clarify atypical brain lesions in OSMS by neuroimaging and pathological studies. For brain MRI, 124 consecutive Japanese patients with clinically definite MS based on Poser criteria were enrolled, 57 with OSMS and 67 with CMS. Ten autopsied cases (seven OSMS and three CMS) were studied pathologically. Although the frequency of brain lesions fulfilling Barkhof criteria was significantly higher in CMS than in OSMS, periventricular linear lesions along with the anterior portion of the corpus callosum and the lateral ventricles were significantly more common in OSMS than in CMS. Pathologically, periventricular lesions in CMS extended deeply into the white matter, while those in OSMS were confined to periventricular areas. T cell infiltration in lesions was prominent in CMS but not in OSMS. Although severe axonal loss and cavity formation were commonly seen in periventricular and spinal cord lesions in OSMS, lymphocytic infiltrates and vessel wall thickening were observed only in the latter. Thus, we suggested that anterior periventricular linear lesions without ovoid ones are characteristic of OSMS. Multiple Sclerosis 2008; 14: 343—353. http://msj.sagepub.com

Keywords

MRI multiple sclerosis optic-spinal periventricular

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References

Kira J. Multiple sclerosis in the Japanese population. Lancet Neurol 2003; 2: 117-27.

Kira J. , Kanai T. , Nishimura Y. , Yamasaki K. , Matsushita S. , Kawano Y. et al. Western versus Asian types of multiple sclerosis: immunogenetically and clinically distinct disorders. Ann Neurol 1996; 40: 569-74.

Yamasaki K. , Horiuchi I. , Minohara M. , Kawano Y. , Ohyagi Y. , Yamada T. et al. HLA-DPB1*0501-associated opticospinal multiple sclerosis: clinical, neuroimaging and immunogenetic studies. Brain 1999; 122: 1689-96.

Kurtzke JF Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983; 33: 1444-52.

Wingerchuk DM , Hogancamp WF , O'Brien PC , Weinshenker BG The clinical course of neuromyelitis optica (Devic's syndrome). Neurology 1999; 53: 1107-14.

Cree BAC , Goodin DS , Hauser SL Neuromyelitis optica . Semin Neurol 2002; 22: 105-22.

Lucchinetti CF , Mandler RN , McGavern D. , Bruck W. , Gleich G. , Ransohoff RM et al. A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica . Brain 2002; 125: 1450-61.

Lennon VA , Wingerchuk DM , Kryzer TJ , Pittock SJ , Lucchinetti CF , Fujihara K. et al. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 2004; 364: 2106-12.

Chong HT , Ramli N. , Lee KH , Kim BJ , Ursekar M. , Dayananda K. et al. Magnetic resonance imaging of Asians with multiple sclerosis was similar to that of the West. Neurol Asia 2004; 9: 47-53.

10.

Minohara M. , Matsuoka T. , Li W. , Osoegawa M. , Ishizu T. , Ohyagi Y. et al. Upregulation of myeloperoxidase in patients with opticospinal multiple sclerosis: positive correlation with disease severity. J Neuroimmunol 2006; 178: 156-60.

11.

Su J-J. , Osoegawa M. , Minohara M. , Tanaka M. , Ishizu T. , Mihara F. et al. Upregulation of vascular growth factors in multiple sclerosis: correlation with MRI findings . J Neurol Sci 2006; 243: 21-30.

12.

Nakashima I. , Fujihara K. , Miyazawa H. , Misu T. , Fujimori J. , Sato S. et al. Relevance of callosal and periventricular MRI findings to oligoclonal bands in multiple sclerosis. Acta Neurol Scand 2005; 113: 125-31.

13.

Barkhof F. , Filippi M. , Miller DH , Scheltens P. , Campi A. , Polman CH et al. Comparison of MRI criteria at first presentation to predict conversion to clinically definite multiple sclerosis. Brain 1997; 120: 2059-69.

14.

Pittock SJ , Lennon VA , Krecke K. , Wingerchuk DM , Lucchinetti CF , Weinshenker BG Brain abnormalities in neuromyelitis optica. Arch Neurol 2006; 63: 390-6.

15.

Pittock SJ , Weinshenker BG , Lucchinetti CF , Wingerchuk DM , Corboy JR , Lennon VA Neuromyelitis optica brain lesions localized at sites of high aquaporin-4 expression. Arch Neurol 2006; 63: 964-8.

16.

Lennon VA , Kryzer TJ , Pittock SJ , Verkman AS , Hinson SR IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 2005; 202: 473-7.

17.

Poser CM , Paty DW , Scheinberg L. , McDonald WI , Davis FA , Ebers GC et al. New diagnostic criteria for multiple sclerosis: guidelines for research protocols. Ann Neurol 1983; 13: 227-31.

18.

Fukazawa T. , Hamada T. , Tashiro K. , Moriwaka F. , Yanagihara T. Acute transverse myelopathy in multiple sclerosis . J Neurol Sci 1990; 100: 217-22.

19.

Paty DW , Oger JJF , Kastrukoff LF , Hashimoto SA , Hooge JP , Eisen AA et al. MRI in the diagnosis of MS: a prospective study with comparison of clinical evaluation, evoked potentials, oligoclonal banding, and CT. Neurology 1988; 38: 180-5.

20.

Wingerchuk DM , Lennon VA , Pittock SJ , Lucchinetti CF , Weinshenker BG Revised diagnostic criteria for neuromyelitis optica. Neurology 2006; 66: 1485-9.

21.

Ishizu T. , Osoegawa M. , Mei F. -J, Kikuchi H. , Tanaka M. , Takakura Y. et al. Intrathecal activation of the IL-17/IL-8 axis in opticospinal multiple sclerosis. Brain 2005; 128: 988-1002.

22.

Nagra RM , Becher B. , Tourtellotte WW , Antel JP , Gold D. , Paladino T. et al. Immunohistochemical and genetic evidence of myeloperoxidase involvement in multiple sclerosis. J Neuroimmunol 1997; 71: 97-107.

23.

Osoegawa M. , Niino M. , Ochi H. , Kikuchi S. , Murai H. , Fukazawa T. et al. Platelet-activating factor acetylhydrolase gene polymorphism and its activity in Japanese patients with multiple sclerosis . J Neuroimmunol 2004 ; 150: 150-6.

24.

Papadopoulos MC , Manley GT , Krishna S. , Verkman AS Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J 2004 ; 18: 1291-3.

25.

Aoki-Yoshino K. , Uchihara T. , Duyckaerts C. , Nakamura A. , Hauw J. - J. Wakayama Y. Enhanced expression of aquaporin-4 in human brain with inflammatory diseases. Acta Neuropathol (Berl) 2005; 110: 281-8.

26.

Nakashima I. , Fujihara K. , Miyazawa I. , Misu T. , Narikawa K. , Nakamura M. et al. Clinical and MRI features of Japanese MS patients with NMO-IgG. J Neurol Neurosurg Psychiatry 2006; 77: 1073-5.

27.

Shiraki H. , Yamamoto T. , Hamada S. Pathoanatomical studies on neuromyelitis optica and demyelinating myelitis in Japan. Seishinshinkeigakuzasshi 1958; 60: 1121-57.

28.

Okinaka S. , Tsubaki T. , Kuroiwa Y. , Toyokura Y. , Imamura Y. Multiple sclerosis and allied diseases in Japan; clinical characteristics . Neurology 1958; 8: 756-63.

29.

Tabira T. , Tateishi J. Neuropathological features of MS in Japan. In Kuroiwa Y , Kurland LT eds. Multiple sclerosis East and West. Fukuoka : Kyushu University Press, 1982 : 273-95.